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August 2022; 12 (4) Research Article

Predictors of Disease Activity and Worsening in Relapsing-Remitting Multiple Sclerosis

Yinan Zhang, Stacey Cofield, Gary Cutter, Stephen Krieger, Jerry S. Wolinsky, Fred Lublin
First published May 12, 2022, DOI: https://doi.org/10.1212/CPJ.0000000000001177
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Article Information

vol. 12 no. 4 e58-e65
DOI: 
https://doi.org/10.1212/CPJ.0000000000001177
Published By: 
Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology
Print ISSN: 
2163-0402
Online ISSN: 
2163-0933
History: 
  • Received December 13, 2021
  • Accepted April 11, 2022
  • First Published May 12, 2022.

Article Versions

Copyright & Usage: 
© 2022 American Academy of Neurology

Author Disclosures

    1. Yinan Zhang, MD,
    2. Stacey Cofield, PhD,
    3. Gary Cutter, PhD,
    4. Stephen Krieger, MD,
    5. Jerry S. Wolinsky, MD and
    6. Fred Lublin, MD
  1. Yinan Zhang, MD,
    2. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. (1) National Multiple Sclerosis Society

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  2. Stacey Cofield, PhD,
    3. Scientific Advisory Boards:

    1. (1) Department of Defense (2) JMP Discovery Summit Advisory Board

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. (1) Oxford University Press, reviewer textbook, 2016

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. National Multiple Sclerosis Society, NARCOMS

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  3. Gary Cutter, PhD,
    4. Scientific Advisory Boards:

    1. Data and Safety Monitoring Boards: AI Therapeutics, AMO Pharma, Astra-Zeneca, Avexis Pharmaceuticals, Biolinerx, Brainstorm Cell Therapeutics, Bristol Meyers Squibb/Celgene, CSL Behring, Galmed Pharmaceuticals, Green Valley Pharma, Immunic, Mapi Pharmaceuticals LTD, Merck, Merck/Pfizer, Mitsubishi Tanabe Pharma Holdings, Opko Biologics, Novartis, Regeneron, Sanofi-Aventis, Reata Pharmaceuticals, Teva pharmaceuticals, VielaBio Inc, , NHLBI (Protocol Review Committee), NICHD (OPRU oversight committee).

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. Multiple Sclerosis Journal: editorial board, (11 yrs); Multiple Sclerosis and Related Disorders: Editorial board; (1 yr);Am journal of the Society of Nephrology. Statistical editor; contributing statistical help (6 yrs); Alzheimer's and Dementia (5) yrs; Neurology Clinical Practice (7yrs recently ended);

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. Alexion, Antisense Therapeutics, Biogen, Clinical Trial Solutions LLC, Genzyme, Genentech, GW Pharmaceuticals, Immunic, Klein-Buendel Incorporated, Medimmune/Viela Bio/Horizon Pharmaceuticals, Merck/Serono, Neurogenesis LTD, Novartis, Osmotica Pharmaceuticals, Perception Neurosciences, Protalix Biotherapeutics, Recursion/Cerexis Pharmaceuticals, Regeneron, Reckover Pharmaceuticals, Roche.Therapeutics.

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. President of Pythagoras Inc. a consulting company

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. U01 AR071133 (Bammam) 12/6/2016 – 11/30/2022 6 calendar NIH/NIAMS $ 6,942,009 (total funds) The Exercise and Physical Activity Collaborative Team (ExPact): A Proposed MoTrPAC Clinical Center The goals are to help lead the NIH Common Fund initiative – Molecular Transducers of Physical Activity Consortium (MoTrPAC) – by serving as one of six adult clinical centers conducting a large-scale, randomized, controlled trial (RCT) of resistance vs. aerobic exercise training vs. no-exercise control. The RCT will be complemented by molecular acute response studies in RCT participants as well as highly trained athletes; all with the goal of generating molecular maps that reveal key underpinnings of exercise-induced health benefits. No Number (Motl) 01/01/2020 – 06/30/2021 .87 calendar Consortium of Multiple Sclerosis Centers $39,996 total costs Examining Patterns and Correlates of Wellness in Persons with Multiple Sclerosis who use Wheelchairs 5U54NS115054 (PI: Kaminski, sub-PI: Cutter) 09/01/2019 – 05/31/2024 0.6 calendar NIH/NINDS $321,265 total costs Rare Disease Network for Myasthenia Gravis We propose development of the Myasthenia Gravis Clinical Research Consortium (MGNet) to coordinate investigators in collection of detailed clinical information and biological specimen along with performance of pilot investigations of a therapeutic and biomarker discovery. We link our efforts to a program to develop new investigators in myasthenia gravis. This is all done with the purpose of enhancing performance clinical trials and care of patients to one day find a cure for myasthenia gravis. 5R01AG057684 (Kennedy) 09/15/2017 – 03/31/2022 0.12 calendar NIH/NIA $3,242,015 total costs In Silico Screening of Medications for Slowing Alzheimer's Disease Progression In this proposal, we will explore drug repurposing, in which medications approved to treat other illnesses are evaluated for potential benefits in Alzheimer's disease (AD), to improve the efficiency of the drug development process, which currently ends in failure for most candidate medications despite considerable investment of both time and resources. We will apply data mining, or pattern recognition, algorithms to the concomitant medications taken by subjects in previous AD clinical trials that are part of our meta-database of more than 6,500 individuals and by participants in Medicare Part D with more than 787,000 individuals. This approach will allow us to screen hundreds of drugs for effects in slowing the progression of AD, which will guide future clinical trials of novel therapeutic agents. 1U01HL119242 (PI: Szychowski) 09/01/2014 – 11/30/2021 .96 calendar NIH/NHLBI $2,744,642 total costs Chronic Hypertension and Pregnancy (CHAP): Data Coordinating Center CHAP is a pragmatic multi-center randomized trial of pregnant women with mild chronic hypertension to evaluate the benefits and harms of antihypertensive therapy to a goal <140/90 mmHg (as recommended for the general population in the US) compared with ACOG's current policy of expectant management of mild chronic hypertension in pregnancy. The trial will enroll 2,404 women across more than 60 clinical sites. R01HD098132-01A1 (PI: Subramaniam) 01/20/2020 – 12/31/2024 .24 calendar NIH/NICHD $3,242,752 total costs Childhood Pulmonary and Related Outcomes after Perinatal Exposure to Adjunctive Azithromycin Prophylaxis for Cesarean Delivery (C/SOAP Follow-Up Study) We propose a US multi-center long-term follow-up study of children from the parent C/SOAP trial at age 6-8 years to evaluate childhood respiratory and gastrointestinal health effects after perinatal exposure to adjunctive azithromycin; findings from this study will be used to inform and strengthen national and global health care policy regarding the use of adjunctive azithromycin to reduce maternal infection after cesarean delivery. R01AI148359 (PI: Geisler) 05/11/2020 – 04/30/2025 0.6 calendar NIH/NIAID $3,201,254 total costs Host Immune Responses to Chlamydia trachomatis Candidate Vaccine Antigens and their Association with Clinical Correlates of Protective Immunity in Women Current chlamydia prevention and control efforts have been unable to reduce chlamydia infection rates, which provides strong rationale for development of a chlamydia vaccine to prevent chlamydia and its reproductive sequelae. This project will evaluate systemic and mucosal cellular and humoral immune responses induced by promising chlamydia vaccine candidate antigens and will assess association of the immune responses with clinical correlates of protection against chlamydia in women (spontaneous clearance of chlamydia and absence of reinfection after treatment). Findings may advance chlamydia vaccine development efforts and lead to formulation of these candidate antigens into a chlamydia vaccine for a phase I study. 5U01NS092595 (PI: Bebin) 06/01/2016 – 05/31/2022 0.24 calendar NIH/NINDS $7,084,395 total costs Preventing Epilepsy Using Vigabatrin in Infants with Tuberous Sclerosis Complex This study focuses on the developmental impact of early vigabatrin treatment in infants with Tuberous Sclerosis Complex who are at risk of developing epilepsy. Also, the study aims to determine the effectiveness of early vigabatrin treatment in clinical seizure prevention and its impact on the development of drug resistant epilepsy at 24months of age. This is the first seizure prevention trial in patients with TSC in the United States. 1R01HD088646 (PI: Katheria, sub PI: Szychowski) 04/01/2017- 03/31/2022 0.6 CM NIH/NCHHD $547,854 (total funds) Premature Infants Receiving Cord Milking Or Delayed Cord Clamping Delayed cord clamping reduces overall bleeding in the brain of premature infants, but not the most severe types. “Milking” the umbilical cord, a method used to transfer blood from the placenta into the baby before the umbilical cord is clamped, may provide additional blood volume to the brain and other vital organs thereby reducing bleeding in the brain and improving long-term outcomes in premature babies. This study will determine whether umbilical cord milking reduces bleeding in the brain or death in premature newborns delivered by Cesarean section compared to delaying clamping of the umbilical cord. P30DK079337 (PI: Agarwal) 08/01/2018 – 07/31/2023 1.77 CM NIH/NIDDK $1,136,699 (total funds) O'Brien Center for Acute Kidney Injury Research Acute kidney injury (AKI) is a major cause for morbidity and mortality in hospitalized patients and is being increasingly recognized as a cause for chronic kidney disease. AKI doubles the length of stay in the hospital, increasing health care resources. The UAB-UCSD O'Brien Center has brought together a team of investigators to serve unmet needs of our investigator base and to fill the gaps in knowledge in the field of AKI and AKI-related research. K23HD091849 (Gerstenecker) 09/12/2018 – 08/31/2023 0 calendar, Co-Mentor NIH/NICHHD $630,875 total costs Investigating the Impact of Cognition on Capacity in Multiple Sclerosis At a time in which increased cognitive ability is needed to make complex financial and medical decisions, people with MS are often experiencing cognitive decline; surprisingly though, research into the ability of people with MS to make complex financial and medical decisions is rare. This study proposes to investigate financial and medical decisional capacity and its clinical and neuroanatomical correlates in people with relapsing- remitting MS and progressive MS. The ultimate value of this research will be to act as a necessary first-step in the development of a targeted capacity rehabilitation program for people diagnosed with MS. K23HL127100 (Lebensburger) 04/01/2015 – 03/31/2021 0 calendar, Mentor NIH/NHLBI $916,445 total costs Chronobiology and Chronopharmacology to Prevent Sickle Cell Nephropathy Hypertension is a known risk factor for stroke in sickle cell disease and in other diseases associated with adverse cardiovascular outcomes. Within the context of a feasibility trial, this proposal will develop vital background data to understand the acceptability of, adherence to, and dosing strategy for losartan prior to conducting a definitive trial for adolescent sickle cell disease patients with abnormal circadian blood pressure. A prospective cohort study will also be conducted to define the relationship of urine and blood biomarkers on the development of abnormal nocturnal blood pressure dipping and kidney injury. PENDING OSP 532909 (Lal) 04/01/2022 – 03/31/2027 0.6 CM NIH $935,194 Optimization of Saturation Targets and Resuscitation Trial (OptiSTART) R34HL157412 (Leesar) 04/01/2021 – 03/31/2024 0.6 CM NIH/NHLBI $668,250 total costs Effects of Crushed Ticagrelor and no Fentanyl Versus Eptifibatide Bolus+Ticagrelor and Fentanyl in Patients with NSTE-ACS Undergoing Early PCI: A randomized Trial (CTEP trial) R21HD104996 (Rogers) 09/01/2021 – 08/31/2023 0.6 CM NIH $408,375 total costs Microbiome as a Novel Mechanism of Exercise Training Effects in Multiple Sclerosis R01HL154109 (Sanders) 04/01/2021 – 03/31/2026 0.6 CM NIH/NHLBI $2,929,087 total costs Dietary Sodium & Potassium and Aortic Stiffness R01TR003741 (Danila) 04/01/2021 – 03/31/2024 0.6 CM NIH/NCATS $2,937,048 total costs Digital Health for Rheumatology Care in COVID19 Era OSP 532630 (Motl) 06/01/2021 – 05/31/2024 0.6 CM Bristol-Myers Squibb Foundation, Inc. $770,799 total costs Exercise Promotion and Outcomes Among African-Americans with Multiple Sclerosis Living in Rural Communities OSP 533051 (Leesar) 04/01/2022 – 03/31/2025 0.6 CM NIH/NHLBI $668,250 total costs Platelet Inhibition with Crushed Ticagrelor versus Eptifibatide Bolus in Patients with Non-ST-Segment Elevation Myocardial Infarction undergoing Ad Hoc PCI with no Opiods R01HD108618 (Taub) 04/01/2022 – 03/31/2024 0.6 CM NIH/NCHHD $1,183,924 total costs A Therapy for Long COVID Brain Fog and Cognitive Impairment U24HL155807 (Aban) 07/01/2021 – 06/30/2027 0.6 CM NIH/NHLBI $1,844,073 total costs 2/2 Video Telehealth Pulmonary Rehabilitation to Reduce Hospital Readmission in Chronic Obstructive Pulmonary Disease (Tele-COPD) R01AG070049 (Taub) 08/01/2021 – 07/31/2025 0.6 CM NIH/NCHHD $2,312,394 total costs Transferring Speed of Processing Gains to Everyday Cognitive Tasks after Stroke R01DK131079 (Novak) 12/01/2021 – 11/30/2026 1.2 CM NIH/NIDDK $3,764,635 total costs Unraveling Clinical and Pathophysiologic Disparities in African Americans with IgA Nephropathy) To address the historic lack of research into this chronic disease in African American patients, we will identify the first large, well-characterized, cohort of African American patients with IgA nephropathy and will assess factors associated with their disease pathogenesis, severity, and progression. Role: Co-Investigator K23DK131291 (Farrington) 09/01/2021 – 08/31/2026 no effort, consultant NIH/NIDDK $943,378 The Role of the Immune System in Arteriovenous Fistula Failure OSP 531819 (Agarwal) 06/01/2021 – 05/31/2025 0.6 CM NIH $2,830,956 Biological and Clinical Characterization of Kidney Patients Post-Acute Covid19 (BACKPAC) OTA-21-015B OSP 532702 (Aban) 02/01/2022 – 01/31/2028 0.6 CM NIH $281,882 Early Epilepsy Surgery in Tuberous Sclerosis Complex

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. The MG Registry receives funding from the Myasthenia Gravis Foundation of America

    Stock/Stock Options/Board of Directors Compensation:

    1. Consortium of MS Centers - Past President - only expenses covered

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  4. Stephen Krieger, MD,
    5. Scientific Advisory Boards:

    1. (1) Yale, DSMB (2) TG Therapeutics, Adjudication Committee (3) EMD Serono, Adjudication Committee

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. (1) Biogen - honoraria for non-promotional lectures (2) EMD Serono - honoraria for non-promotional journal club (3) Genentech - honoraria for non-promotional lectures

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. (1) Biogen, (2) EMD Serono, (3) Genentech, (4) Novartis, (5) Octave, (6) Genzyme/Sanofi,(7) TG Therapeutics

    Speakers' Bureaus:

    1. (1) Biogen, non-promotional speaker, (2) EMD Serono, non-promotional speaker, (3) Genentech, non-promotional speaker

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. (1) Biogen, (2) Novartis, (3) BMS

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  5. Jerry S. Wolinsky, MD and
    6. Scientific Advisory Boards:

    1. Compensation for service on steering committees or data monitoring boards for Avotres, Brainstorm Cell Therapeutics, Cleveland Clinic Foundation, EMD Serono, MedDay Pharmaceuticals, Novartis/Sandoz, Roche/Genentech, Sanofi/Genzyme and University of Alabama Birmingham.

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. Honoraria, travel support and expenses were provided from Roche for CME related activities.

    Editorial Boards:

    1. NONE

    Patents:

    1. US010363245B2; Board of Regents UT System; Methods for treating CNS lesions

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. Royalties are received for monoclonal antibodies out-licensed through the University of Texas Health Science Center at Houston to Millipore (Chemicon International) Corporation since 1993.

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  6. Fred Lublin, MD
    7. Scientific Advisory Boards:

    1. Biogen; EMD Serono; Novartis; Teva; Actelion; Sanofi/Genzyme; Acorda; Roche/Genentech; MedImmune/ Viela Bio; Receptos/Celgene; Medday; Atara Biotherapeutics; Mapi Pharma; Innate Immunotherapeutics; Apitope; Orion Biotechnology; Brainstorm Cell Therapeutics; Jazz Pharmaceuticals; GW Pharma; Mylan; Immunic; Population Council; Avotres; Janssen, BMS; Neurogene; Banner Life Sciences; Labcorp; Entelexo Biotherapeutics; Neuralight; SetPoint Medical

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. Most, if not all, consulting activity and scientific boards listed above and below involved travel, all before March 2020, that was either paid for directly or reimbursed.

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. Same as Advisory Boards

    Speakers' Bureaus:

    1. Sanofi Genzyme- non-promotional EMD Serono- non-promotional

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. Novartis; Biogen; Sanofi, NMSS, NIH; Brainstorm Cell Therapeutics

    Research Support, Government Entities:

    1. 1) NIH/NINDS- PI, 2018-2022 2) NIH/NINDS- PI, 2018-2022

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. 1) National Multiple Sclerosis Society- PI, 2014-2019 2) National Multiple Sclerosis Society- PI 2019-2024

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. Stock Options- Avotres; Neuralight

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. I have provided occasional expert testimony in various matters

  1. Department of Neurology (YZ), The Ohio State University Wexner Medical Center, Columbus; Department of Biostatistics (SC, GC), University of Alabama at Birmingham; Department of Neurology (SK, FL), Icahn School of Medicine at Mount Sinai, New York; and Department of Neurology (JSW), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth).
  1. Correspondence
    Dr. Zhang yinan.zhang{at}osumc.edu
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